Deciphering the symbiotic life of marine plankton

Plankton is an essential part of life on earth, producing half of the oxygen of our atmosphere and regulating global climate. Many planktonic organisms live in intimate symbiosis but scientists still do not know much about the underlying mechanisms. Using several techniques, including X-ray fluorescence imaging at the ESRF, an international team of scientists has shed light into the metabolism of the symbiotic life of marine plankton at the subcellular level.

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Symbiosis between eukaryotic planktonic hosts and microalgae (photosymbiosis) is a widespread and ecologically important phenomenon in the ocean. It is essential for colonization of nutrient-scarce sunlit waters and could increase in future oceans with the expansion of zones poor in nutrients.

Despite its importance, the way by which hosts integrate and accommodate microalgal cells in the symbiotic process is still unknown. Johan Decelle, from the Helmholtz Institute and the University Grenoble Alpes, investigated the transition between free-living and symbiotic stage of a key microalga called Phaeocystis. He joined forces with researchers from the ESRF, the Institute de Biologie Structurale, the CNRS, CEA, the Royal Netherlands Institute for Sea Research, Sorbonne Universités, the INRA and the EMBL Heidelberg in his quest to study this symbiosis at the subcellular level using cutting-edge high-resolution microscopy techniques.

Plankton’s samples are not straightforward to study. Decelle first had to go out to sea in the Mediterranean Sea to collect plankton in symbiosis, with the assistance of the Marine Station (Laboratoire d´Oceanographie de Villefrance sur Mer, LOV) . The team then cryo-fixed and prepared the living cells at the Institute de Biologie Structurale, on the same site as the ESRF, to get the sample ready for the beamlines. Sections of cells were then analyzed at beamlines ID21 and ID16B, with X-ray fluorescence to unveil the distribution and concentration of metals, such as iron and cobalt. They combined these with other complementary techniques, namely 3D electron microscopy for the cell architecture, and nanoSIMS and ToF-SIMS to visualize the allocation of nitrogen, phosphorous and sulfur.

The results were unexpected: “We have discovered a new mode of photosymbiosis, which does not correspond at all to what is observed in corals or lichens for example", says Johan Decelle. "Within the host, microalgae undergo a radical transformation of their structural organization and their metabolism. This transformation, presumably induced by the host, maximizes the photosynthetic activity of the algae." Increased photosynthetic performance is linked to increased algal cell volume, multiplication of voluminous chloroplasts and of their photosynthetic membranes. The X-ray analyses on ID21 and ID16B showed that the iron concentration in symbiotic algae is higher compared to the same algal cell in free-living phase (outside the host) and is particulary stored in vacuoles. This suggests that the host delivers a substantial amount of iron, which is one of the most important elements for photosynthesis in the ocean.

The researchers noted that the nutrients inside the cells show that the nitrogen to phosphorus ratio significantly increases in the symbiotic microalgae, indicating higher investment into the light-energy acquisition machinery rather than growth. The results suggest that this widespread and abundant planktonic symbiosis is rather an algal farming strategy of the host and pave the way for more studies to further understand the molecular mechanisms behind the images.

"These results represent a radical change in the understanding of the functioning of a key symbiotic relationship of marine ecosystems" concludes Johan Decelle. "It also brings new hypotheses to try to understand what happened during evolution: how can a host take control of an alga and integrate a photosynthetic function."

Reference:

Decelle J. and al. Algal remodeling in a ubiquitous planktonic photosymbiosis, Current biology, 28 February 2019.